Neurobehavioral Inhibition of Reward‐driven Feeding: Implications for Dieting and Obesity

The development of effective weight loss interventions requires a thorough understanding of the motivational factors that drive and inhibit the overconsumption of food. Obesity was once believed to result purely from disruptions of homeostatic mechanisms controlling food intake. However, it is increasingly recognized that much of the excess caloric intake in obesity is driven by pleasure or the rewarding properties of readily available palatable food (1,2). It is important to note that the motivation underlying this reward-driven or “hedonic” feeding appears to have a different neurophysiological basis than homeostatic controls over energy balance, though the hedonic and homeostatic systems do interact (3). Recently, a surge of research has linked the appetitive motivation to consume palatable food to activation of the mesolimbic dopaminergic system, a neural pathway also implicated in drug addiction and addictive behaviors such as gambling (4). As a result of these findings, a view of obesity as a “disorder of appetitive motivation” has gained prominence among a growing number of obesity researchers. However, a model of hedonic feeding based purely on appetitive motivation has limitations, including an inability to explain instances of feeding behavior parsimoniously in both dieters and nondieters. The aim of this review is to summarize the strengths and weaknesses of the appetitive model, present the extant literature linking control of hedonic feeding to inhibitory processes localized in the prefrontal cortex (PFC), and delineate a theoretical model in which hedonic feeding is viewed as the product of an interaction between appetitive motivation and inhibitory control. The human feeding system leaves room for dessert. Humans will continue to consume palatable food even after energy requirements have been met and homeostatic satiety signals have been engaged. This consumption is clearly not driven by an acute need for calories, and hedonic factors (taste, pleasure, reward) play a large role in this type of feeding. Simply stated, the hedonic feeding model holds that palatable food consumption in the absence of an energy deficit (or the physiological signals associated with energy deficit) is driven by an appetitive motivational state referred to as “hedonic hunger” (2), and not by homeostatic controls over feeding. (For discussion of the role of reward in homeostatic feeding, which may be subjectively associated with escape from hunger rather than the pleasant tastes and textures of palatable food, see ref. (5).) Hedonic feeding has an evolutionary basis. Modern humans preferentially overconsume sweet and high-fat palatable foods (6). Hominids subsisted as hunter-gatherers for the majority of evolutionary history and access to these types of foods (e.g., fruits, animal meat) was presumably limited. Hunting or prolonged foraging would often have been required to obtain sweet and high-fat foods, and it is likely that the capacity to find these foods pleasurable and highly rewarding motivated ancestral humans to engage in these food-seeking behaviors. After expending many calories to obtain them, consuming palatable foods in excess of one's current need for calories would have allowed some energy to be stored as fat, which could buffer against starvation in instances of short-term food shortage or famine. Thus, the ability of palatable food to promote overconsumption by overriding satiety signals was preserved in our species (3,7). In modern times, when palatable food is abundant and accessible, our evolutionarily derived capacity for hedonic feeding has contributed to an epidemic of overconsumption and obesity. Hedonic feeding is driven by both sensory and motivational processes that also play a role in drug addiction. The sensory pleasure resulting from tasting and ingesting palatable foods (and drugs) has been referred to as “liking.” Liking is distinct from the motivational process of “wanting,” which refers to the incentive value of a stimulus (8). Although humans generally want the foods they like, and like the foods that they want, liking and wanting have separate neurophysiological underpinnings and are dissociable under several circumstances. For example, drug-addicted individuals report a greater desire to consume a drug over time despite a gradual decrease in the degree to which they find consumption pleasurable, and selective lesioning of the neural system underlying wanting (described below) results in animals who show affective facial expressions of pleasure upon tasting palatable foods but are unmotivated to obtain them (8). Thus, although the sensory process of liking and the motivational process of wanting typically converge with respect to individual foods, instances of dissociation indicate separate neural underpinnings. Some have suggested that wanting plays a stronger role in obesity than liking given that obese individuals do not consistently appear to derive greater pleasure from tasting and ingesting palatable foods (1). Liking of palatable foods is believed to be mediated by opioid neurotransmission in the nucleus accumbens (9), and pharmacological manipulation of this area results in dramatic changes in animals' intake of palatable foods and their affective facial expressions to the tasting of palatable food (10). In distinction, wanting has been consistently linked to activation of the mesolimbic system, which includes dopaminergic projections from the ventral tegmental area to the nucleus accumbens (8) (see special issue of Psychopharmacology (vol. 191, issue 3) for perspectives on the functions of mesolimbic dopamine). Ingestion of palatable food triggers dopamine release in the nucleus accumbens (11), and genetic or neurochemical manipulations of the mesolimbic system influence the motivation to consume palatable food without affecting its perceived pleasantness (liking) (12,13). Connections from the nucleus accumbens to hypothalamic feeding centers provide a pathway through which palatable food can influence feeding behavior by overriding satiety signals (3). As several authors have articulated (especially refs. (9,14)), the mesolimbic system underlies the motivational drive to consume both palatable food and drugs of abuse, and it seems that drugs of abuse “hijack” the endogenous reward system that evolved to promote hedonic feeding and other motivated behavior. Additional findings also suggest overlap in the neural mediation of hedonic feeding and drug addiction. For example, animal studies have shown that repeated consumption of sugar can produce behavioral withdrawal effects similar to abstinence from addictive drugs (e.g., motor agitation, anxiety (15)). Second, cravings to consume both addictive drugs and palatable food increase with exposure to drug or palatable food cues (respectively), and the mechanism underlying both effects appears to involve cue-induced activation of the mesolimbic system (16,17). Finally, the reinforcing values of both palatable food and addictive drugs increase following psychological stress, which may involve sensitization of the mesolimbic system by stress-induced activation of the hypothalamic-pituitary-adrenocortical axis (19) (see ref. (18) for discussion of stress and reward-driven feeding). Together, the biobehavioral parallels between drug addiction and hedonic feeding have substantiated the view that hedonic feeding represents an “addictive behavior” driven by heightened wanting of palatable food. Several lines of research suggest that both sensitization and desensitization of the appetitive system can explain individual differences in hedonic feeding. Questionnaire measures of reward sensitivity correlate positively with neural activation of striatal reward centers in response to exposure to palatable food cues (20) and have been used to quantify individual differences in appetitive motivation. Self-reported reward sensitivity is also positively associated with reported food craving and BMI (21). Individual differences in appetitive motivation can also be characterized at the neuronal or even the genetic level. Adiposity has been associated with reduced density of striatal dopamine D2 receptors in obese individuals (22), suggesting neurophysiological hyposensitivity to reward. To compensate for this hyposensitivity, individuals with this phenotype are thought to overconsume palatable foods to achieve stronger stimulation of the reward circuit. Similarly, Epstein and colleagues (23) reported that individuals with the TaqI A1 allele of the dopamine D2 receptor, which has previously been linked to deficient dopaminergic reward processing, obesity, and addiction (24), find snack foods more reinforcing than those without this polymorphism. Together, these findings indicate that individual differences in appetitive motivation evaluated at multiple levels of analysis explain engagement in hedonic feeding. However, as discussed below, the appetitive model is less useful for explaining instances in which hedonic feeding does not occur. How do dieters regularly abstain from highly desired (wanted) palatable food, at least for finite periods of time? Can dieting be explained within the appetitive model? Given that one's favorite foods do not immediately become less desired on the first day of a diet, it seems that dietary restraint is the product of active inhibitory control of feeding rather than the passive result of reduced appetitive motivation. In fact, active inhibition of hedonic feeding is reflected not only in instances of successful dietary restraint, but also in the manner in which dietary control breaks down. Studies with chronic dieters (“restrained eaters”) show that acute stressful and nonstressful challenges often result in increased food intake (25,26). The most parsimonious explanation is that inhibitory control of hedonic feeding is disrupted during challenges (through mechanisms discussed later), thereby disinhibiting the appetitive motivation to engage in hedonic feeding. Given the large number of individuals struggling to control their weight through dieting, it is important to develop an understanding of the neurobehavioral processes that mediate hedonic feeding inhibition. The notion that inhibitory processes play an important role in feeding is not a novel idea, at least among the lay public. The view that overeating results from a lack of willpower or poor self-control is surprisingly prevalent, and has had the unfortunate consequence of promoting stigmatization of overweight and obese individuals. In addition to its scientific value, systematic investigation of the role of inhibitory control in hedonic feeding will hopefully redirect attention away from the “character” of overweight and obese individuals and toward the biological and environmental factors that influence feeding behavior. Curiously, the scientific understanding of hedonic feeding inhibition is only just beginning to emerge. At this early stage, tentative answers to three key questions about hedonic feeding inhibition can be gleaned from the existing literature. 1. Which evolutionary pressures favored the capacity to inhibit hedonic feeding? 2. What nervous system structures mediate hedonic feeding inhibition? 3. How does hedonic feeding inhibition manifest in cognitive and affective processes? As mentioned earlier, hedonic feeding likely evolved to promote the storage of energy as fat which would buffer against starvation during food shortages. The dramatic rise in obesity prevalence in modern times characterized by readily available palatable food is widely attributed to this evolutionary adaptation. However, the notion that hedonic feeding was generally adaptive for ancestral humans does not preclude the possibility that inhibiting hedonic feeding on a situational basis may also have been adaptive. In other words, the human feeding system may have evolved to follow the “standing rule” to increase fat stores through hedonic feeding when opportunities arose, but to make exceptions to this rule (i.e., inhibit hedonic feeding) in certain circumstances. One can imagine several scenarios in which hedonic feeding inhibition would have been adaptive for ancestral humans. For example, the ability to inhibit hedonic feeding would have allowed one to conserve food during periods of anticipated food shortage (27), such as during prolonged expeditions in nonproductive areas or periodic (e.g., seasonal) reductions in food availability. 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